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Bryozoan Growth and Environmental Reconstruction by Zooid Size Variation

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Bryozoan Growth and Environmental Reconstruction by Zooid Size Variation Vol. 430: 133–146, 2011 MARINE ECOLOGY PROGRESS SERIES Published May 26 doi: 10.3354/meps08965 Mar Ecol Prog Ser Contribution to the Theme Section ‘Evolution and ecology of marine biodiversity’ OPENPEN ACCESSCCESS Bryozoan growth and environmental reconstruction by zooid size variation Beth Okamura1,*, Aaron O’Dea2, 3, Tanya Knowles4 1Department of Zoology, Natural History Museum, London SW7 5BD, UK 2Center for Tropical Paleoecology and Archeology, Smithsonian Tropical Research Institute, Apartado 0843-03092 Panamá, República de Panamá 3Department of Earth and Ocean Sciences, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada 4Department of Earth Science and Engineering, Imperial College London, London SW7 2BP, UK ABSTRACT: The modular growth of cheilostome bryozoans combined with temperature-induced variation in module (zooid) size has enabled the development of a unique proxy for deducing sea- sonal temperature regimes. The approach is based on measures of intracolonial variation in zooid size that can be used to infer the mean annual range of temperature (MART) experienced by a bryozoan colony as predicted by a model of this relationship that was developed primarily to infer palaeosea- sonal regimes. Using the model predictions effectively requires a highly strategic approach to char- acterise the relative amount of within-colony zooid size variation (by adopting random or very sys- tematic measurements of zooids that meet a stringent set of criteria) to gain insights on temperature variation. The method provides an indication of absolute temperature range but not the actual tem- peratures experienced. Here we review the development of, support for and applications of the zooid size MART approach. In particular, we consider the general issue of why body size may vary with temperature, studies that validate the zooid size–temperature relationship and insights that have been gained by application of the zooid size MART approach. We emphasise the potential limitations of the approach, including the influence of confounding factors, and highlight its advantages relative to other proxies for palaeotemperature inferences. Of prime importance is that it is relatively inex- pensive and quick and allows a direct estimate of temperature variation experienced by an individ- ual colony. Our review demonstrates a strong and growing body of evidence that the application of the zooid size MART approach enables robust interpretations for palaeoclimates and merits broad recognition by environmental and evolutionary biologists and climate modellers. KEY WORDS: Cheilostomes · Mean annual range of temperature · MART · Body size–temperature relationship · Palaeoclimates Resale or republication not permitted without written consent of the publisher INTRODUCTION continuous record of growth and the sequential devel- opment of discrete and measurable features that vary Patterns of growth in plants and animals have long consistently with respect to a single environmental been used to gain insights into past environments. variable and remain fixed, thereby permitting the Variable accretion of structural material in trees, fish retrieval of environmental conditions relevant to par- otoliths and the shells of bivalve or gastropod molluscs, ticular time periods. Benthic colonial invertebrates for example, can be used to retrospectively extract can provide an especially appropriate system for such ambient environmental conditions such as rainfall, retrieval, since, with some exceptions (e.g. sponges), temperature or food availability (e.g. Falcon-Lang they comprise distinct, individual modules (zooids) that 2005, Zazzo et al. 2006, Hallmann et al. 2009). Organ- are produced iteratively throughout the lifetime of the ismal attributes that favour such analyses in clude a colony. The sclerochronological analysis of modular *Email: [email protected] © Inter-Research 2011 · www.int-res.com 134 Mar Ecol Prog Ser 430: 133–146, 2011 growth can provide inferences for both intra- and 1989). Once the skeletal walls of a new zooid are interannual environmental variation, information that secreted, there is no further expansion of zooid surface is not readily available from analyses of short-lived, area (O’Dea & Okamura 2000b). This gives the zooid a unitary organisms that are commonly used as proxies, determinate size that has been shown to be controlled such as foraminifers or ostracodes. Furthermore, colo- to a significant extent by the ambient water tempera- niality is often associated with polymorphism, with ture at the time the zooid was produced. Bryozoan modules specialised for different functions within a colonies therefore record the range of temperatures colony. These attributes, viz. modular iteration, poly- experienced during their lifetime as intracolonial vari- morphism and individual colony longevities ranging ation in zooid size (Fig. 1). Such temperature-induced from months to many years, may enable joint insights variation in size is also observed in unitary animals and into environmental conditions and associated life his- is generally known as the ‘temperature–size rule’ tory variation (O’Dea & Okamura 2000a, O’Dea & (Atkinson 1994). Jackson 2002). Such insights are generally difficult to The above-mentioned features make cheilostome achieve through investigations of longer-lived unitary bryozoans unique amongst colonial taxa in offering organisms, such as bivalves or brachiopods, since the opportunities for inferring environmental conditions morphologies of these organisms do not readily pro- and biotic responses in the present day as well as over vide a record of functional allocation during their life- geological time. Other colonial taxa such as corals, time. Surprisingly, however, the unique contribution of hydroids, ascidians and other non-cheilostome bryo - colonial invertebrates for retrospectively deducing zoans either do not produce carbonate skeletons, show environmental and life history variation has not been indeterminate growth of their polyps or zooids, or ex - widely recognised. hibit little to no polymorphism and therefore preclude Bryozoans are colonial, suspension-feeding inverte- gaining additional insights on how life histories may brates that are common members of benthic assem- respond to environmental conditions. blages (McKinney & Jackson 1989). There are some Recognition of the unique opportunities afforded by 6000 described extant species of bryozoans (Gordon cheilostome bryozoans for the retrieval of environmen- et al. 2009), most of which belong to the order tal information led to the development of a method that Cheilostomata. Colonies of cheilostomes comprise allows the estimation of the mean annual range of asexually budded zooids that are reinforced by skele- temperature (MART) based on variation in zooid size tal walls composed of calcitic and/or aragonitic car - within cheilostome colonies. The method is based on bonate (Rucker & Carver 1969, Smith et al. 2004). using model predictions for how zooid size varies with Typically, cheilostomes display zooid polymorphism MART and thus requires that zooids meet a stringent (McKinney & Jackson 1989). The majority of zooids are set of criteria, in keeping with assumptions of the specialised for feeding (autozooids), whilst a smaller model, and that a strategic sampling protocol is adopted proportion function in reproduction (ovicells) and to target appropriate zooids randomly or very system- defense (avicularia). The carbonate skeleton (‘zooe- atically. The method informs on absolute seasonal vari- cium’) confers preservation of colony features, includ- ation in temperature but does not indicate the actual ing zooid polymorphism, and bryozoans are well rep- temperatures. Thus polar and tropical bryozoans will resented in the fossil record (McKinney & Jackson converge on similar low MART values. Fig. 1. Cupuladria exfragminis. Sea- sonal variation in zooid size. Scanning electron micrographs of a recent col - ony from the Gulf of Panama. Size dif- ference between zooids that devel- oped during (A) upwelling (cold) and (B) non-upwelling (warm) conditions. Same magnification for the purpose of comparison. The skeletal walls of both autozooids (large orifices) and avicularia (small orifices) are evident. Scale bar = 150 µm. Photos by R. Dewel Okamura et al.: Environmental reconstruction by zooid size analysis 135 In this paper we describe this zooid size MART cent review). Mechanistic explanations have in cluded: approach, review studies that validate the zooid (1) the production of smaller adult stages be cause size–temperature relationship on which the technique developmental rate is more strongly influenced by in - depends and summarise research that has made use of creasing temperature than growth rate (van der Have the approach in order to demonstrate the insights that & de Jong 1996); (2) the related hypotheses that cell can be gained by its adoption. We also emphasise the (van Voorhies 1996, Woods 1999) or body (Chapelle & potential limitations of the zooid size MART approach, Peck 1999) size is limited by oxygen diffusion. describe confounding factors that must be borne in Atkinson et al. (2006) recently addressed the ex - mind and suggest directions for future studies. How- planation that the temperature–size relationship may ever, because the approach is based on temperature- relate to oxygen concentrations by examining the ther- induced variation in zooid size, we first describe the mal responses of the bryozoan Celleporella hyalina to
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